Having finished 2 of the 3 peer reviews I've been asked to write lately, I figured I might as well do some post-publication review. Discussion is welcome!
John Bois & Stephen J. Mullin (2017): Dinosaur nest ecology and predation during the Late Cretaceous: was there a relationship between upper [sic] Cretaceous extinction and nesting behavior? Historical Biology online early: 11 pp. DOI: 10.1080/08912963.2016.1277423
The paper does not, as I feared, proclaim "mammals ate all their eggs" as the only cause of extinction; it offers this as one of several factors that happened to coincide in time and therefore caused the mass extinction together. It does not, however, try to quantify the contribution of this factor (or that of any other factor).
More generally, it hardly tries to quantify anything.
That's quite a pity. A population of tetrapods can sustain its numbers if just over two of the eggs a female lies in its lifetime result in hatchlings that survive to reproductive age. Table 3 cites a reference saying that 95 % of ostriches die in their first year (it isn't mentioned if this is counted from hatching or from egg-laying). Given such and similar numbers, it should be possible to estimate, with reasonable error margins, how many eggs a *Triceratops* female may have had to lay in a lifetime, given the terminal Cretaceous array of potential predators on eggs and hatchlings, so that two would on average result in reproductive adults. If that number is ridiculously high (say, 30,000 eggs in 15 years), well, then we're looking at a likely cause of extinction! But such a test, or any hint of one, is absent from the paper.
== The appearance of mammalian nest predators ==
I wondered about the gobiconodontids. John, are you still here? Over the years, you've discussed your hypothesis several times, and I remember bringing up the gobiconodontids several times; I don't remember getting an explanation for why they didn't singlehandedly wipe out most dinosaurs from Laurasia in the Aptian or so. The paper doesn't contain one either. It doesn't even try. The following paragraph from p. 4:
"There is evidence that non-avian dinosaurs had always experienced egg and hatchling predation by mammals (Hu et al. 2005), varanids, and crocodilians, as well as other dinosaurs (Ruxton et al. 2014; and references therein). One could argue that, because they had survived under that predatory regime, non-avian dinosaurs could respond similarly to an increased diversity of birds, mammals, and snakes. However, the large body size of non-avian dinosaurs conferred the disadvantage of relatively long generation times. Therefore, their ability to adapt quickly to sudden changes in their environment was decreased (Hone & Benton 2005). We suggest that additional environmental pressure from a growing guild of offspring predators would cause unsustainable attrition of offspring."
contains the only mention of gobiconodontids: Hu et al. (2005) is the paper on *Psittacosaurus* hatchlings as stomach content of *Repenomamus*. That's it. On the other 10 pages there isn't a whiff of a hint of them; they are brought up and promptly forgotten.
The argument in that paragraph is that large egg-layers can't adapt to sudden increases in the amount of egg/hatchling predators, because they're large and therefore have too long generation times. So far, so good! However, the application of this argument to the K-Pg mass extinction rests on two unspoken assumptions: that the supposed rise of large eutherians, metatherians, multituberculates and gondwanatheres in the Maastrichtian was sudden by this measure, and that the appearance and diversification of the gobiconodontids in the early Aptian was not sudden. Not only aren't these assumptions mentioned, they aren't defended either (explicitly or implicitly, let alone with any numbers).
The Berriasian through Barremian terrestrial fossil record isn't terribly good, so, while the appearance and diversification of the gobiconodontids looks sudden enough to me, I can't say that it actually was. At least some of the large mammals of the Maastrichtian, however, have some history behind them. Table 1 features *Didelphodon* and cites Wilson et al. (2016) for it; yet, that same paper provides a handy overview in its fig. 3 which shows that *Didelphodon* and its fellow stagodontid *Eodelphis* go back deep into the Campanian. There's nothing sudden about the rise of large stagodontid metatherians! We're talking about more than 10 million years before the end of the K here. Further, table 1 features *Nanocuris*; that's a deltatheroidan, and the large deltatheroidan *Deltatheridium* goes back at least as far.
The same table misspells *Yubaatar*; and the reference for *Altacreodus*, Fox (2015), is missing from the references list. It is:
Richard C. Fox (2015): A revision of the Late Cretaceous–Paleocene eutherian mammal Cimolestes Marsh, 1889. Canadian Journal of Earth Sciences 52: 1137–1149. DOI: 10.1139/cjes-2015-0113
At the other end of the Cretaceous, we find *Triconodon mordax*, probably as bitey as its name says, which was the size of a cat (lower-jaw length = 8 cm). Ground-nesting dinosaurs lived with large carnivorous mammals the whole Cretaceous, which lasted longer than the entire time that has passed since its end. And yet these same mammals are supposed to have made a noticeable contribution to doing them in?
And never mind the Cretaceous. Table 1 gives the masses of *Altacreodus* and *Nanocuris* as 565 and 523 g. *Castorocauda* from the Middle Jurassic has been estimated to 500–800 g, and *Sinoconodon* from the Early Jurassic to up to 500 g.
== The appearance of avian nest predators ==
The diversification of "ornithurine" (euornithean) birds in the Late Cretaceous is mentioned in a confused three-paragraph section that also mentions the extinction of nonavian dinosaurs and the extinction of non-"ornithurine" dinosaurs, but not the extinction of non-neornithean euornitheans. No attempt is made to show that any Cretaceous euornitheans were potential nest predators, or that any enantiornitheans were not potential nest predators; no attempt is made to show that any Cretaceous euornitheans nested in trees or that any enantiornitheans did not. Nothing is quantified.
== The appearance of ophidian nest predators ==
There's *Sanajeh* in sauropod nests at the very top of the Cretaceous. The authors point out the presence of other madtsoiids in "Madagascar, Patagonia, Spain and France" before acknowledging that the Romanian *Nidophis insularis* was probably a bit to small to do any damage to the hadrosaur nests it was found in. Well. The fossil record of madtsoiids is not good enough that we could tell when and where madtsoiids started preying on sauropod nests, or how quickly they spread. (An SVP presentation last year associated Madtsoiidae and *Dinilysia*...) What we can say for sure is that many dinosaur eggs were too small for *Sanajeh* and that whole continents (North America in particular) appear to have remained madtsoiid-free.
== Large ground-nesting birds in the Cenozoic ==
According to the paper's main hypothesis, there shouldn't be any large ground-nesting birds in the presence of Cenozoic levels of nest predation. Therefore the paper hypothesizes that all large Cenozoic ground-nesting birds have lived in environments that provided protection against nest predation – although no attempt is made to quantify how much protection that is.
Ostriches, emus and phorusrhacids are explained away as being tied to grasslands. Fair enough, if we grant that eggs are exceptionally hard to find in grasslands (see below). Rheas and dromornithids are also explained away as being tied to grasslands. Problem is, the Paleocene rhea *Diogenornis* lived at a time when grasslands simply didn't exist yet, and the same holds in Australia for all Eocene and Oligocene dromornithids. Brontornithids are not mentioned.
The existence of cassowaries, moas and kiwis is interestingly blamed on supposed lack of predation on the adults, not on the eggs and hatchlings. The aepyornithids are mentioned in the same paragraph, while a later one blames their existence on wetlands. Wetlands are also made responsible for the Paleocene/Eocene wide distribution and subsequent extinction of the gastornithids, because wetlands hinder "access by mammalian predators" (with references that all seem to be about small birds; "waterfowl" and "the purple swamphen" are mentioned in 2 of the 4 titles). I do have to wonder: you can't just lay an elephant-bird egg into a swamp...? And what kind of "wetland" is it that is too muddy to allow herpestids or oxyaenids to simply walk into it, but not muddy enough that a quarter-ton bird would get stuck? Mordor is supposed to be rather dry...? I'm aware that at least one species of aepyornithid was apparently called vorompatra, meaning "swamp bird" (vorona + patra), but that doesn't mean it was able to nest like a duck or a sedge warbler. Further, gastornithids are known from all three northern continents; were there really enough "wetlands" for them to nest in and nonetheless spread around the Earth?
The Paleogene European "ratites" (*Palaeotis*, *Remiornis*, *Eleutherornis*) are not mentioned, and neither is *Eremopezus* from Fayûm. Messel was full of mammals and crocodiles (in fact, I have no idea how the adults of the _small_ flightless bird *Messelornis* managed to survive), and Fayûm was a scary environment with potential nest predators up to and including *Gigantophis*.
Finally, from the "Wetlands" section on p. 8, let me quote this gem: "_*Aepyornis*_. The elephant bird (~500 kg) likely owed its success to the existence of wetland habitat for nesting; wetland contraction is implicated in the extinction of *Aepyornis* (Heuvelmans 2014)." That's the whole paragraph. Yes, you may trust your eyes: the only cited source is a posthumous reprint (not marked as such in the references list!) of the famous cryptozoological work from 1955 (English translation 1958). (Heuvelmans died in 2001.) Catastrophic wetland contraction throughout this huge island within the last thousand years, right at the same time when humans settled the place? Some of the paleontology in Heuvelman's book was probably already outdated in 1955, and yet it's uncritically cited in Historical Biology in 2017. (Note also that *Mullerornis* is not even implicitly mentioned; not all Holocene aepyornithids are *Aepyornis*.)
Back to grasslands. P. 7: "Ratites might be analogous to non-avian dinosaurs in that, unlike their adult forms, their eggs and juveniles are susceptible to predation by a wide range of species and size classes (Tables 2 and 3). Magige et al. (2009) found that all observed nests failed in the Serengeti ecosystem. Predation accounted for 80% of these failures. Studying ostrich reproductive success in Nairobi National Park, Davies (2002) found a 73% failure rate of nests (mainly attributable to predation) and of those chicks that hatched, 88% were taken by predators. Without the concealment property of grasses, this rate might be higher. Indeed, the chicks of both rhea and emu are known to utilize grasses for concealment when danger threatens (Bruning 1974; Davies 2002). This factor is particularly relevant for large oviparous species because the disparity of adult versus hatchling size necessitates that small oviparous offspring spend a proportionally greater period of their early life-history at risk of predation."
Again: "Without the concealment property of grasses, this rate might be higher." Indeed it might. By how much? Would it ever reach 100 %, or 95, or even just 90? No attempt is made to answer this question at all.
The "concealment property of grasses" is supported only by two anecdotes, by the way. I quote the preceding paragraph in full: "James and Olson (1983) argued that flightlessness evolved on islands in the absence of predation. We suggest that grasslands, especially in their more arid ranges, are ‘islands’ of low predator density where large oviparous species can effectively conceal their nests. Bertram (1992) noted that he could not detect an ostrich nest to within 10 m, but that it is sited within a territory of >2 km². Rheas of South America, also nest in grassy open habitat (Bruning 1974) and are similarly inconspicuous (Darwin 1839)." Comparisons to other vegetated landscapes, quantified or anecdotal, are not provided. How easy is it to find a cassowary nest? We aren't told. And, again, why is it that rheas, emus, dromornithids, apparently ostriches (assuming they're related to some or all of the Paleogene European "ratites") and possibly phorusrhacids were already flightless and pretty large before the forests they lived in turned into grasslands?
== You can't run, you can't hide, you can't fight and you can't swamp? ==
Many terrestrial egg-layers today take various measures to reduce predation on their nests: they run, hide, fight, and/or swamp the predators. For dinosaurs above a certain unspecified size, hiding the nest is argued to be impossible because the eggs are just too big and/or the brooding adults (if any) are detectable from afar. (No quantification of course.) "Running" off to an inaccessible location, like a treetop, a cliff or a remote island, requires the ability to fly or at least climb and is thus out of the question for most if not all nonavian dinosaurs. Swamping is apparently considered impossible, because (p. 5):
"Perhaps intrinsic to the idea of multiple unattended clutches, is the idea of predator swamping. We contend that it is unlikely that a colony of dinosaurs could abandon their nests and survive excessive offspring predation by overwhelming or satiating predators. For this strategy to be effective, non-avian dinosaurs would have to limit the intensity of destruction of their offspring by avoiding predation and/or limiting temporal access to their eggs and hatchlings. Reproductive effort by many turtle species benefits from both of these factors and provides a relevant contrast to nonavian dinosaur nesting ecology because, even when discovered, the contents of turtle nests swamp predators (Santos et al. 2016)."
As far as I can tell, "we contend that it is unlikely" is the entirety of the argument. The concept of predator swamping is mentioned nowhere else in the paper.
On remote nesting I have to say that there are degrees of remoteness. Surely such islands as Egg Mountain and Egg Island afforded _some_ protection? *Maiasaura* did survive the presence of *Gobiconodon* after all.
If we accept that no attainable degree of remoteness is enough and that even a titanosaur nesting colony couldn't swamp nest predators, that leaves nest defense. The authors correctly point out that nest defense can never be perfect (p. 6):
"If dinosaurs actively defended their nests, we question the effectiveness of this strategy in the face of an emerging guild of small predators for at least two reasons: (i) dinosaurs needed to maintain structural integrity of their nests and lacked the capacity to defend them against burrowing animals. As a modern analogy, the hairy armadillo (*Chaetophractus* sp.) burrows beneath the nest of the much larger rhea (*Rhea americana*) parent (Fernandez & Reboreda 1998). While this source of predation causes many nests to fail, rheas have no defensive response to it."
And yet, they still haven't died out. How can that be? It can't be the fact that they nest in grassland – if anything, grassland soil should be easier to dig through than the sand under a rainforest with all those roots in it. I guess that counts as swamping.
"(ii) small [sic] nocturnal predators have an advantage over large diurnal oviparous species. Ostriches that effectively defend the nest from black-backed jackals (*Canis mesomelas*) in the daylight, apparently abandon the nest under similar attack at night (Bertram 1992). Some non-avian dinosaurs might have been nocturnally active (Schmitz & Motani 2011); however, this interpretation has not been widely accepted (e.g. Hall et al. 2011)."
This is followed by evidence for a nocturnal/fossorial origin of mammals and snakes (all with the implication that Mesozoic dinosaurs were nightblind like ostriches). And yet, ostriches aren't extinct either. Is it the grassland this time? But if so, what happens when a fox or dingo or singing-dog or historically a "Tasmanian" "tiger" attacks a cassowary nest at night?
Crocodiles can't really hide their nests or nest in remote places either, so they defend them. This is implied to be insufficient on its own in the following paragraph from p. 7:
"Nest defense is practiced by most species of crocodilians (Somaweera et al. 2013). This represents an exception to our claim that dependence on nest defense cannot be a viable strategy amid extant predators. We argue that crocodilians have experienced a relatively reduced frequency of offspring predation because their hatchlings find refuge in water. Factors such as turbidity and submerged aquatic vegetation probably enhance crocodilian reproductive success in wetlands (Somaweera et al. 2013); and the semi-aquatic habitat is a particularly effective refuge from mammalian predation (Pasitschniak-Arts & Messier 1995)."
Crocodylian hatchlings are, of course, eaten by all sorts of large actinopterygians, large frogs, birds, varanids (often good swimmers) and adult crocodylians. Unsurprisingly, parents guard and defend their hatchlings in the water well after hatching, too. I conclude that hiding is insufficient on its own in this very case and needs to be supplemented by defense. Whether defense would be sufficient on its own isn't testable, because hiding is cheaper.
== What about those that could in fact hide? ==
P. 6: "In comparison to almost all extant terrestrial oviparous vertebrates of <30 kg in body mass, the large size of non-avian dinosaurs precluded stealth when laying and incubating their eggs. We recognize that several small carnivorous non-avian dinosaurs remained into the latest Cretaceous (Turner et al. 2007; Benson et al. 2014; Larson et al. 2016), and that concealment was a likely strategy for them. However, we argue that no single extinction hypothesis can consider every extinct species. Indeed, other scenarios invoke the extinction of carnivorous species following the disappearance of their herbivorous prey (e.g. Alvarez et al. 1980), and we predict a similar fate for the smaller members of the clade Deinonychosauria."
Come on, authors. Don't you agree that the small deinonychosaurs (< 30 kg) were ideally suited to eat the diversifying mammals? Would they really care if the hadrosaurs died out?
I argue that a single hypothesis for the cause of a _mass extinction event_ should – parsimony! –, and indeed can, consider every species that took part in that event. As far as I can tell, the Chicxulub impact has little trouble explaining the extinction of all deinonychosaurs and a whole lot of mammals at the same time as loads and loads of haptophytes and planktonic foraminifera. But I digress.
== Conclusion ==
No, not "epic fail". WAIR was a case of epic fail: a coherent hypothesis that has ended up teaching us a lot about extant and extinct animals with borderline flight capabilities and was slain by one ugly fact, the fact that it requires the ability to lift the wings far dorsal of the shoulder joints. It was a research program; it was useful. Probably we'd already be singing songs about it if that were our culture.*
I was surprised to find that the paper had four reviewers. All of them are anonymous, and any responsible editor is not mentioned (some journals do this, some don't).
BTW, the authors and the reviewers seem to have expected that the manuscript would be copyedited. Of course it wasn't; very few journals do that anymore. Various typos abound, and (as mentioned above) there's at least one missing reference.
* I've long thought that we scientists have become our own tribe with our own culture. Other people have long begun to notice; to avoid a long digression, I'll just mention the secret language called Damin or Demiin – check out the story of why there's any research on it!
== So, why aren't there more large flightless birds in the Cenozoic? ==
Why weren't there more large flightless birds in the Mesozoic, seeing as *Gargantuavis* proves the concept? I suspect the reason is the same: the ecological niches in question were already occupied. In the Cenozoic, mammals mostly happened to get there first; "everything is the way it is because it got that way" (D'A. W. Thompson, 1917: On Growth and Form).